Differential responses of soil bacteria and fungi to altered precipitation in a meadow steppe
Introduction
As an important component of the global water cycle, precipitation patterns are likely to be altered in location-specific ways due to global warming (IPCC, 2007, Knapp et al., 2017). Changes in precipitation will have significant ecological consequences including shifts in community composition and variation in ecosystem functions, especially in water-limited ecosystems such as grasslands (Nielsen and Ball, 2015, Zhang et al., 2019). In semi-arid grasslands, soil microorganisms are the most sensitive community component to the resultant changes in soil water availability (Barnard et al., 2015, Chen et al., 2019) and indirect variation in physicochemical conditions (Ochoa-Hueso et al., 2018, Na et al., 2019). Despite numerous studies that have been conducted on the effects of soil water availability on community composition and activities of soil microbes (Huang et al., 2015, Koyama et al., 2018, Qin et al., 2020), we are still far from fully understanding the responses of belowground microbial community structure and functions to the predicted changes in precipitation. Moreover, few studies have tested the responsivity of soil microbial communities and soil properties to a range of precipitation changes i.e., multiple levels of both increases and decreases, under otherwise identical environmental conditions.
Soil microorganisms are key participants in nutrient mineralization and organic matter decomposition, and an increase or decrease in precipitation directly influences the soil microbial community by changing soil water availability (Ren et al., 2017). Soil microorganisms, including bacteria and fungi, differ in their response to variation in soil water availability. Due to different physiological properties and survival strategies, bacteria typically respond faster than fungi to changes in soil water availability (Engelhardt et al., 2018). Bacterial biomass and diversity responds to increased precipitation and soil water content (SWC) because they are highly dependent on water for movement and substrate diffusion (Harris, 1981). However, it has been reported that osmotic stress accompanying increased SWC can lead to a decrease in bacterial biomass and diversity (Kieft et al., 1987). Previous studies have shown that precipitation can drive changes in the bacterial community via physicochemical variability in SWC and pH (Felsmann et al., 2015, Ochoa-Hueso et al., 2018). On the other hand, Marschner et al., 2003, Sessitsch et al., 2001 found that soil organic matter content, carbon/nitrogen ratio, and soil texture significantly affected the bacterial community. Altered precipitation (especially drought) may drive changes in the composition of the soil carbon (C) pool, with consequences for soil C loss (Hueso et al., 2012), leading to limited capability of bacteria for rapid growth. Despite these prior results, the soil abiotic factors that determine bacterial community composition are far from clear.
In contrast to bacterial communities, multiple studies have reported that precipitation changes could affect soil fungal communities by altering both abiotic and biotic factors (Hawkes et al., 2011, Liu et al., 2018). For instance, fungal richness can be shaped by temperature, SWC, pH, and nitrogen (N) availability (Allison et al., 2007, Bi et al., 2012, Tedersoo et al., 2014, Wang et al., 2015), which all tend to co-vary with changes in precipitation. Alternatively, variation in precipitation may indirectly affect the fungal community by changes in plant community composition, diversity, and productivity (Knapp et al., 2002, Suttle et al., 2007, Prober et al., 2015). For example, plants can influence mycorrhizal fungi via root exudates and shift soil pH within the rhizosphere (Richardson et al., 2009). To date, there is no consensus for how altered precipitation leads to fungal community changes. This is because fungal communities are more resistant than bacteria to water limitation, likely due to their hyphal connections that allow them to be better adapted to water-poor pore domains in soil when searching for nutrient resources (De Boer et al., 2005). These prior responses of bacteria and fungi to soil moisture highlight the need to simultaneously quantify the effects of changes in precipitation on bacteria, fungi, and the soil microenvironment.
Soil microorganisms affect land-atmosphere C exchange, modulating ecosystem C fluxes through decomposition and heterotrophic respiration (Hopkins and Gregorich, 2005, Standing et al., 2005, Zhang et al., 2013). At the same time, grasslands contribute to soil C sinks at a global scale (Poulter et al., 2014, Ochoa-Hueso et al., 2018). In northeast China, grasslands are represented by meadow steppe, which is a part of a widely distributed grassland ecosystem across the Eurasian Steppe region. Global circulation models predict that extreme precipitation events and the intensity of future precipitation will be on the rise in this region (IPCC, 2007, Sun and Ding, 2010). Moreover, Liu et al. (2005) have reported that increased annual precipitation is mainly driven by the increase in extreme precipitation events during the growing season. Therefore, understanding the responses of microbial community biomass, diversity, structure, and activity to variation in precipitation will improve our ability to predict the impacts of precipitation regime change on ecosystem C cycling and feedbacks between ecosystem processes and global climate change.
In this study, we examined the effects of altered precipitation on microbial diversity and community structure using a three-year field experiment with five levels of increasing and decreasing precipitation magnitude. Research was conducted in the Songnen meadow steppe, where ecosystem processes are strongly influenced by large inter-annual precipitation variability (Yang et al., 2020). To identify the patterns and key processes controlling soil microbial community diversity in response to precipitation, we measured plant productivity (e.g., aboveground biomass, belowground biomass), soil abiotic properties (e.g., SWC, soil bulk density, soil water filled pore space, soil total porosity, pH, soil organic carbon, total nitrogen, and total phosphorus), microbial community composition, and diversity and structure (using Illumina sequencing). We hypothesized that: (1) effects of the altered precipitation on soil microbial diversity and activity depend on the annual, ambient precipitation; (2) soil microorganisms (both bacteria and fungi) have an optimal precipitation range for biomass and diversity; and (3) SWC and soil nutrient status are the main factors modulating the microbial diversity in response to precipitation.
Section snippets
Study site
This study was conducted at the Songnen Grassland Ecological Research Station of Northeast Normal University, Jilin Province, northeastern China (44°40′-44°44′N, 123°44′-123°47′E; 160 m in elevation). The study area has a temperate semi-arid monsoon climate. The mean annual air temperature (1950-2014) is 6.3 °C (Zhong et al., 2019) and the mean annual precipitation (1963-2012) is approximately 430 mm. The study site is dominated by Leymus chinensis (Trin.) Tzvel., a C3 perennial rhizomatous
Precipitation patterns
For both experimental years, there was substantial variation in both rainfall event size and seasonal distribution. Despite significant inter-annual differences in the rainfall amount, the precipitation patterns for the two study years were both described as a dry spring with a rainy summer. The amount of rainfall (from April to August sampling date) in 2017 (397.8 mm) was greater than in 2016 (203.6 mm) (Fig. 1a). Considering long-term mean annual precipitation, we defined 2016 as the dry year
Soil microbial activity and biomass, and their response to precipitation magnitude
The precipitation gradient effects were more pronounced in the dry year than in the wet year (SFig. 1). In the dry year, reduced precipitation resulted in soil water scarcity, which constrained plant growth and microbial activity (Delgado-Baquerizo et al., 2013). Lower SWC levels most likely reduced plant transpiration rate, and therefore element uptake (Farooq et al., 2012). The reduced input by plants was likely accompanied by weakened element adsorption capacity of microbes. It is possible
Conclusions
Bacterial diversity and composition were sensitive to the altered precipitation treatments, whereas fungal diversity and composition were highly responsive to inter-annual variation in precipitation. Higher annual precipitation shifted microbial composition from dominance by bacteria to fungi. When shifts in soil microbial communities occurred in response to precipitation, soil water content, total phosphorus, and pH were the most critical drivers, yet the indirect effects of plants also cannot
Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
This study was supported by the National Key Research and Development Program of China (2016YFC0500602), National Natural Science Foundation of China (31570470, 31870456), and the Program of Introducing Talents of Discipline to Universities (B16011). Kai Zhu was supported by the US National Science Foundation grant DEB 1926438. Xuechen Yang acknowledges support from China Scholarship Council (CSC). We especially thank Professor Weixin Cheng at the University of California, Santa Cruz, for his
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